Skip to main content
SpringerLink
Log in

The Induction of Saccharomyces cerevisiae Hsp104 Synthesis by Heat Shock Is Controlled by Mitochondria

  • Published:
Russian Journal of Genetics Aims and scope Submit manuscript

Abstract

Heat shock protein Hsp104 of Saccharomyces cerevisiae functions as a protector of cells against heat stress. When yeast are grown in media containing nonfermentable carbon sources, the constitutive level of this protein increases, which suggests an association between the expression of Hsp104 and yeast energy metabolism. In this work, it is shown that distortions in the function of mitochondria appearing as a result of mutation petite or after exposure of cells to the mitochondrial inhibitor sodium azide reduce the induction of Hsp104 synthesis during heat shock. Since the addition of sodium azide suppressed the formation of induced thermotolerance in the parent type and in mutant hsp104,the expression of gene HSP104 and other stress genes during heat shock is apparently regulated by mitochondria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. Boy-Marcotte, E., Lagniel, G., Perrot, M., et al., The Heat Shock Response in Yeast: Differential Regulations and Contributions of the Msn2p/Msn4p and Hsf1p Regulons, Mol. Microbiol., 1999, vol. 33,no. 2, pp. 274-283.

    Google Scholar 

  2. Sanchez, Y. and Lindquist, S., HSP104 Required for Induced Thermotolerance, Science, 1990, vol. 248,no. 4959, pp. 1112-1115.

    Google Scholar 

  3. Ferreira, P.C., Ness, F., Edwards, S.R., et al., The Elimination of the Yeast [PSI+] Prion by Guanidine Hydrochloride Is the Result of Hsp104 Inactivation, Mol. Microbiol., 2001, vol. 40,no. 6, pp. 1357-1369.

    Google Scholar 

  4. Jung, G. and Masison, D.C., Guanidine Hydrochloride Inhibits Hsp104 Activity in Vivo: A Possible Explanation for Its Effect in Curing Yeast Prions, Curr. Microbiol., 2001, vol. 43,no. 1, pp. 7-10.

    Google Scholar 

  5. Newnam, G.P., Wegrzyn, R.D., Lindquist, S.L., and Chernoff, Y.O., Antagonistic Interactions between Yeast Chaperones Hsp104 and Hsp70 in Prion Curing, Mol. Cell. Biol., 1999, vol. 19,no. 2, pp. 1325-1333.

    Google Scholar 

  6. Chernoff, Y.O., Lindquist, S.L., Ono, B., et al., Role of the Chaperone Protein Hsp104 in Propagation of the Yeast Prion-like Factor [psi +], Science, 1995, vol. 268,no. 5212, pp. 880-884.

    Google Scholar 

  7. Wegrzyn, R.D., Bapat, K., Newnam, G.P., et al., Mechanism of Prion Loss after Hsp104 Inactivation in Yeast, Mol. Cell. Biol., 2001, vol. 21,no. 14, pp. 4656-4669.

    Google Scholar 

  8. De Deken, R.H., The Crabtree Effect: A Regulatory System in Yeast, J. Gen. Microbiol., 1966, vol. 44,no. 2, pp. 149-156.

    Google Scholar 

  9. Sanchez, Y., Taulien, J., Borkovich, K.A., and Lindquist, S., Hsp104 Is Required for Tolerance to Many Forms of Stress, EMBO J., 1992, vol. 11,no. 6, pp. 2357-2364.

    Google Scholar 

  10. Slonimski, P.P., Perrodin, G., and Croft, J.H., Ethidium Bromide-Induced Mutation of Yeast Mitochondria: Complete Transformation of Cells into Respiratory Deficient Non-Chromosomal “Petites,” Biochem. Biophys. Res. Commun., 1968, vol. 30,no. 3, pp. 232-239.

    Google Scholar 

  11. Lowry, O.H., Rosebrough, N.J., Farr, A.L., and Randall, R.J., Protein Measurement with the Folin Phenol Reagent, J. Biol. Chem., 1951, vol. 193,no. 1, pp. 265-275.

    Google Scholar 

  12. Timmons, T.M. and Dunbar, B.S., Protein Blotting and Immunodetection, Methods Enzymol., 1990, vol. 182, pp. 679-688.

    Google Scholar 

  13. Gauze, G.F. and Kuzovkova, L.I., Themperature Sensitivity of Respiration-Deficient Mutants of Yeast, Izv. Akad. Nauk SSSR, Ser. Biol., 1970, vol. 26,no. 2, pp. 305-308.

    Google Scholar 

  14. Traven, A., Wong, J.M., Xu, D., et al., Interorganellar Communication: Altered Nuclear Gene Expression Profiles in a Yeast Mitochondrial DNA Mutant, J. Biol. Chem., 2001, vol. 276,no. 6, pp. 4020-4027.

    Google Scholar 

  15. Rikhvanov, E.G., Varakina, N.N., Rusaleva, T.M., et al., Respiratory Changes in Yeast Saccharomyces cerevisiae Exposed to Heat Shock, Mikrobiologiya, 2001, vol. 70,no. 4, pp. 531-535.

    Google Scholar 

  16. Weitzel, G., Pilatus, U., and Rensing, L., The Cytoplasmic pH, ATP Content and Total Protein Synthesis Rate during Heat Shock Protein-Inducing Treatments in Yeast, Exp. Cell Res., 1987, vol. 170,no. 1, pp. 64-79.

    Google Scholar 

  17. Wilson, D.F. and Chance, B., Azide Inhibition of Mitochondrial Electron Transport: I. The Aerobic Steady State of Succinate Oxidation, Biochim. Biophys. Acta, 1967, vol. 131,no. 3, pp. 421-430.

    Google Scholar 

  18. Rikhvanov, E.G., Varakina, N.N., Rusaleva, T.M., et al., The Effect of Sodium Azide on Heat Shock Resistance of Yeasts Saccharomyces cerevisiae and Debaryomyces vanriji, Mikrobiologiya, 2001, vol. 70,no. 3, pp. 300-304.

    Google Scholar 

  19. Rikhvanov, E.G., Varakina, N.N., Rusaleva, T.M., et al., Sodium Azide Reduces the Thermotolerance of Respiratively Grown Yeasts, Curr. Microbiol., 2002, vol. 45,no. 6, pp. 394-399.

    Google Scholar 

  20. Ashburner, M. and Bonner, J.J., The Induction of Gene Activity in Drosophila by Heat Shock, Cell (Cambridge, Mass.), 1979, vol. 17,no. 2, pp. 241-254.

    Google Scholar 

  21. Sanchez, Y., Parsell, D.A., Taulien, J., et al., Genetic Evidence for a Functional Relationship between Hsp104 and Hsp70, J. Bacteriol., 1993, vol. 175,no. 20, pp. 6484-6491.

    Google Scholar 

  22. Wieser, R., Adam, G., Wagner, A., et al., Heat Shock Factor-Independent Heat Control of Transcription of the CTT1 Gene Encoding the Cytosolic Catalase T of Saccharomyces cerevisiae, J. Biol. Chem., 1991, vol. 266,no. 19, pp. 12 406-12 411.

    Google Scholar 

  23. Sugiyama, K., Izawa, S., and Inoue, Y., The Yap1p-Dependent Induction of Glutathione Synthesis in Heat Shock Response of Saccharomyces cerevisiae, J. Biol. Chem., 2000, vol. 275,no. 20, pp. 15 535-15 540.

    Google Scholar 

  24. Weber, J. and Senior, A.E., Effects of the Inhibitors Azide, Dicyclohexylcarbodiimide, and Aurovertin on Nucleotide Binding to the Three F1-ATPase Catalytic Sites Measured Using Specific Tryptophan Probes, J. Biol. Chem., 1998, vol. 273,no. 50, pp. 33 210-33 215.

    Google Scholar 

  25. Parsell, D.A., Kowal, A.S., Singer, M.A., and Lindquist, S., Protein Disaggregation Mediated by Heat-Shock Protein Hsp104, Nature, 1994, vol. 372,no. 6505, pp. 475-478.

    Google Scholar 

  26. Sugiyama, K., Kawamura, A., Izawa, S., and Inoue, Y., Role of Glutathione in Heat Shock-Induced Cell Death of Saccharomyces cerevisiae, Biochem. J., 2000, vol. 352, part 1, pp. 71-78.

    Google Scholar 

  27. Estruch, F., Stress-Controlled Transcription Factors, Stress-Induced Genes and Stress Tolerance in Budding Yeast, FEMS Microbiol. Rev., 2000, vol. 24,no. 4, pp. 469-486.

    Google Scholar 

  28. Lindquist, S. and Kim, G., Heat-Shock Protein 104 Expression Is Sufficient for Thermotolerance in Yeast, Proc. Natl. Acad. Sci. USA, 1996, vol. 93,no. 11, pp. 5301-5306.

    Google Scholar 

  29. Thevelein, J.M. and de Winde, J.H., Novel Sensing Mechanisms and Targets for the cAMP-Protein Kinase A Pathway in the Yeast Saccharomyces cerevisiae, Mol. Microbiol., 1999, vol. 33,no. 5, pp. 904-918.

    Google Scholar 

  30. Bussereau, F., Dupont, C.H., Boy-Marcotte, E., et al., The CCS1 Gene from Saccharomyces cerevisiae Which Is Involved in Mitochondrial Functions Is Identified as IRA2, an Attenuator of RAS1 and RAS2 Gene Products, Curr. Genet., 1992, vol. 21,nos. 4–5, pp. 325-329.

    Google Scholar 

  31. Thevelein, J.M., Beullens, M., Honshoven, F., et al., Regulation of the cAMP Level in the Yeast Saccharomyces cerevisiae: Intracellular pH and the Effect of Membrane-Depolarizing Compounds, J. Gen. Microbiol., 1987, vol. 133, part 8, pp. 2191-2196.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Siberian Institute of Plant Physiology and Biochemistry, Siberian Division, Russian Academy of Sciences, Irkutsk, 664033, Russia

    E. G. Rikhvanov, E. I. Rachenko, N. N. Varakina, T. M. Rusaleva, G. B. Borovskii & V. K. Voinikov

Authors
  1. E. G. Rikhvanov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. I. Rachenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. N. Varakina
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. T. M. Rusaleva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. B. Borovskii
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. K. Voinikov
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rikhvanov, E.G., Rachenko, E.I., Varakina, N.N. et al. The Induction of Saccharomyces cerevisiae Hsp104 Synthesis by Heat Shock Is Controlled by Mitochondria. Russian Journal of Genetics 40, 341–347 (2004). https://doi.org/10.1023/B:RUGE.0000024969.45581.ad

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:RUGE.0000024969.45581.ad

Keywords

Search

Navigation